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Within the state of Alabama from Birmingham north to Decatur, this highway is sometimes called the "Decatur Highway." From Birmingham south to Montgomery, US 31 is sometimes called the "Montgomery Highway." South of Montgomery, US 31 is sometimes called the "Mobile Highway". Markers in North Alabama also identify it as the "Beeline Highway".

In downtown Birmingham, with I-20/I-59 is also the northwestern terminus of US 280 in Alabama. US 31 and US 280 travel together along the Red Mountain Expressway Cut (the "Elton B. Stevens" Expressway), leading to the southern and southeastern suburbs of Birmingham.

Well north of Birmingham, US 31 shares the roadway with I-65 between Blount Springs (exit 289) and Hayden (exit 287) because US 31's roadway was converted back in the early 1960s to I-65 to cross several ridgelines of the southwestern Appalachian Mountains. This highway, which was ungraded to Interstate Highway standards, was the first stretch of Interstate Highway to be opened to traffic in Alabama.

US 31 and I-65 also share the roadway for 14 miles (23 km) from mile marker 354 in Athens, Alabama, to Tennessee's mile marker 1 in Ardmore. There are no highway signs confirming this in either state on this stretch, aside from the directional signs at the entrance ramps in Athens and Ardmore. However, this is shown on the official highway maps of both states. The original roadway of US 31 between the two locations still exists as State Route 251 (SR 251) in Alabama and SR 7 in Tennessee between Athens and Ardmore.

US 31E stays east of I-65, passing through Glasgow and Bardstown. It enters Louisville from the southeast, where it is named Bardstown Road for most of its length in the city.

US 31W closely follows I-65 from the Tennessee state line, through Bowling Green, to Elizabethtown. From here, it diverges to the west and passes through Fort Knox. North of Fort Knox, US 31W joins with US 60 in Kentucky and it roughly follows the Ohio River into Louisville. In southwestern Louisville, US 31W is called Dixie Highway. It is the major commercial street in this area.

Before the Interstate era, US 31 was a major north–south highway. I-65 supplanted US 31 and either US 31W or US 31E as a through route between Mobile and Indianapolis. South of Indianapolis, all segments of US 31 not traveling concurrently with I-65 have been reduced to roads largely of local use. I-196 now carries the route of US 31 between Holland, and St. Joseph, Michigan. All of US 31 between Indianapolis and Ludington, Michigan, is divided highway—some of it is freeway, including a bypass route of South Bend, Indiana. The segment between Indianapolis and South Bend is scheduled for upgrade or replacement with Interstate-standard freeway. Environmental impact studies have shown that the fifth phase of the then-to-be-constructed freeway segment between Napier Avenue near Benton Harbor, Michigan, and I-94 may not be complete until 2015.

The portion of I-75 north of US 31's northern terminus toward the Mackinac Bridge was designated part of US 31 prior to the 1990s and was US 31's northernmost portion to be built to freeway status. Since its truncation at the I-75 interchange, however, the northernmost segment of the US 31 freeway ends near Ludington.

In Alabama, US 31 follows portions of the Pulaski Pike beginning at the Alabama–Tennessee State line at Ardmore, and was originally routed on what is now called Alabama State Route 257 (SR-257). It follows roughly along the Decatur Stage Road to the site of Rhodes Ferry in Decatur, and also intersected and follows portions of the Stouts Road to Birmingham. From Birmingham, it follows portions of the Columbiana Road and roughly parallels it in Hoover along the present widened route and intersects with the Ashville-Montevallo Road or the Cahaba Trail (SR-119) and follows it on a branch to Calera. US 31, beginning in Chilton County, follows a branch of the Talladega-Montgomery Stage Road, a road that went from Talladega and went south from Columbiana to near present-day Clanton, Verbena, and Montgomery, and was operated by Jemison, Ficklin, & Powell, who operated stagecoaches on the road. US 31 in Prattville came to the site of Reese's Ferry on the Alabama River, where it was replaced by the present bridge near Prattville. From Montgomery, US 31 follows parts of the Federal Road, and is presently routed on the Greenville Branch of the Federal Road, and follows the Montgomery-Mobile Road through Conecuh, and Escambia Counties and also intersects with the Pensacola Trading Path or the "Old Wolf Trail" from Burnt Corn.

At its southern end, US 31 originally traveled further west than it currently does, passing through Spanish Fort, Alabama. It crossed Mobile Bay via several narrow bridges, including the Admiral Raphael Semmes Bridge, a drawbridge spanning the Tensaw River. It turned north along the east bank of the Mobile River, crossing the river into Plateau, over the former Cochrane Bridge, another old drawbridge where the current Cochrane–Africatown USA Bridge is now located. It then turned south to end at US 90. It now officially ends at US 98 in Spanish Fort.